Occurrence of fishy off-flavor in cow's milk
Fishy off-flavor in milk is a quality defect recently observed in bulk milk in Sweden, which causes considerable losses to both milk producers and dairy companies. Statistical data from an investigation made 1999 regarding the occurrence of off-flavor in milk showed that out of roughly 2,100 herds, 115 (i.e. >5%) had received one or more complaints about fishy off-flavor in bulk milk. Altogether, these 115 herds had received 242 complaints about a moderate fishy off-flavor, whereas 18 bulk milk samples were classified as having a pronounced fishy odor/taste. Exact figures on the current prevalence of fishy odor among Swedish dairy cows are difficult to estimate as no routine organoleptic testing on milk from individual cows is performed. However, when random samples of bulk milk from individual farms were judged to have a fishy off-flavor, tests on samples from individual cows were sometimes performed. These tests have shown that the off-flavor most often originates from one or a few cows within a herd. In order to exceed the threshold above which the test panel perceives a fishy off-flavor in the farm bulk milk, a sufficiently high proportion of the total milk must come from affected cows. Consequently, an individual cow with a fishy off-flavor in the milk will go undetected unless she belongs to a fairly small herd. The above figure of 5% is thus likely an underestimate of the problem. To what extent this off-flavor occurs in other countries is not known, as the vast majority do not perform regular tests for off-flavor in bulk milk at the farm level. There are so far no indications that the defect has any fatal effects on traits subjected to natural selection, like calf survival, or traits included in the breeding goal for milk production.
Characteristics
Fishy off-flavor is characterized by a distinct, unpleasant taste and smell, reminiscent of rotting fish. A fishy smell in milk (Humphriss, 1953; Corfield, 1955) and coffee cream (Eyer et al. 1990) has previously been reported in connection with bacterial degradation of lecithin, choline, and betaine, the latter two being intermediate products in the breakdown of lecithin to trimethylamine (TMA) oxide with TMA as an intermediate compound. A further potential source of fishy taint was related to selective oxidation of butterfat (Swoboda & Peers, 1977). The human nose is extremely sensitive to the TMA odor (Ayesh & Smith, 1990), e.g. the olfactory threshold for detection in milk lies around 1-2 ppm (Metha et al. 1974; von Gunten et al. 1976). As a consequence, milk from a few affected cows in a herd has been shown to be sufficient to cause a fishy off-flavor to the whole bulk milk. There have been a few reports on fishy odor in milk related to TMA content in milk from cows on wheat pasture (Metha et al. 1974; von Gunten et al. 1976; Kim et al. 1980).
Similar Phenomena in Other Species
Problems with fishy odor associated with elevated TMA levels have been described in human (‘Fish-odor syndrome’ or ‘Trimethylaminuria’, OMIM #602079, http://www.ncbi.nim.nih.gov) and chicken (Hobson-Frohock et al. 1973). In human, abnormal secretion of TMA has been observed in breath, urine, sweat, saliva, and vaginal secretions (Humbert et al. 1970), whereas in chicken the TMA has predominantly been found in egg yolk (Hobson-Frohock et al. 1973). The TMA is derived from the intestinal degradation of food/feed components rich in TMA or its precursors. Under normal conditions the TMA produced is oxidized to the odor—and tasteless compound TMA-oxide by the liver enzyme flavin-containing monooxygenase (FMO) (Hiavica & Kehl, 1977). The TMA oxide is thereafter excreted in the urine (Al Waiz et al. 1987a). The fishy odor is a consequence of impaired oxidation of TMA (Pearson et al. 1979; Spellacy et al. 1979).
Genetic Causes
The fishy odor shows a recessive mode of inheritance in human (Al-Walz et al. 1987b, 1987c; Ayesh et al. 1993) whereas in chicken it is described as ‘semidominant’ because the expression has been shown to be dependent on the ingestion of e.g. rapeseed meal (Bolton et al. 1976). In human, parents heterozygous for the defect were shown to excrete elevated amounts of TMA in the urine when given oral doses of 600 mg TMA (Al-Waiz et al. 1987c, 1989; Ayesh et al. 1990, 1993). However, in none of the cases did the treatment result in a fishy odor.
The fishy odor syndrome in humans has recently been shown to be due to mutations in FMO3 encoding an isoform of flavin-containing monooxygenase (Dolphin et al. 1997b; Treacy et al. 1998; Akerman et al. 1999; Basarab et al. 1999; Forrest et al. 2001). The gene has been localized to chromosome 1q23-q25 (http://www.ncbi.nim.nih.gov/LocusLink, August 2001) and its genomic sequence is known (Dolphin et al. 1997a). The human FMO3 gene contains one non-coding and 8 coding exons and is 22.5 kb long. (GenBank AH006707, GenBank AL021026)
Dietary Causes
The elevated concentration of TMA observed in various tissues in human, chicken, and cattle is likely to be due to a combination of genetic and dietary effects. Feed components rich in TMA precursors such as betaine, choline and sinapin, are beet products, green leaves and cereals, and rapeseed products. A high intake of these products may result in an accumulation of TMA, which in turn overloads the enzyme system. Rapeseed also contains progoitrin, a substance that in chicken has been shown to act as an FMO inhibitor by competing with TMA for the enzyme's active binding site (Pearson et al. 1982). In humans, the major source of TMA is marine fish and other seafoods (Zhang et al. 1999).